The molecular pathways that trigger the initiation of embryogenesis after fertilization in flowering plants, and prevent its occurrence without fertilization, are not well understood1. Here we show in rice (Oryza sativa) that BABY BOOM1 (BBM1), a member of the AP2 family2 of transcription factors that is expressed in sperm cells, has a key role in this process. Ectopic expression of BBM1 in the egg cell is sufficient for parthenogenesis, which indicates that a single wild-type gene can bypass the fertilization checkpoint in the female gamete. Zygotic expression of BBM1 is initially specific to the male allele but is subsequently biparental, and this is consistent with its observed auto-activation. Triple knockout of the genes BBM1, BBM2 and BBM3 causes embryo arrest and abortion, which are fully rescued by male-transmitted BBM1. These findings suggest that the requirement for fertilization in embryogenesis is mediated by male-genome transmission of pluripotency factors. When genome editing to substitute mitosis for meiosis (MiMe)3,4 is combined with the expression of BBM1 in the egg cell, clonal progeny can be obtained that retain genome-wide parental heterozygosity. The synthetic asexual-propagation trait is heritable through multiple generations of clones. Hybrid crops provide increased yields that cannot be maintained by their progeny owing to genetic segregation. This work establishes the feasibility of asexual reproduction in crops, and could enable the maintenance of hybrids clonally through seed propagation5,6.
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Whole-genome DNA sequencing data for S-Apo line 1 mother plant, the four progeny clones from two generations, and the Kitaake wild-type control are available from National Center for Biotechnology Information (NCBI) BioProject number PRJNA496208. RNA sequencing data from previously published datasets11,15 are available from the NCBI Short Read Archive as Project SRP119200 and from the NCBI Gene Expression Omnibus under accession number GSE50777.
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We thank U. Vijayraghavan for providing pUN and pUGN vectors; S. Kappu, Z. Liechty and C. Santos-Medellín for advice and help with flow cytometry and sequence analysis; B. Van Bockern for rice transformations; and B. Nguyen and A. Yalda for technical assistance, including genotyping and transplantation. This research was supported by research grants from the National Science Foundation (NSF) (IOS-1547760) and the Innovative Genomics Institute to V.S., NSF grant IOS-1810468 to B.Y., National Institutes of Health grant 1S10OD010786-01to the University of California-Davis Genome Center, and by the United States Department of Agriculture Agricultural Experiment Station (project number CA-D-XXX-6973-H). R.M. acknowledges support from the LabEx Saclay Plant Sciences-SPS (ANR-10-LABX-0040-SPS) to the Institut Jean-Pierre Bourgin.
Nature thanks T. Dresselhaus and the other anonymous reviewer(s) for their contribution to the peer review of this work.
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Horticulture Research (2018)